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Effect of exogenous insulin and fasting on growth hormone receptor and IGF-I expression in the pre-ovulatory follicle of ewes

Published online by Cambridge University Press:  31 March 2011

A. Schneider ,
L. F. M. Pfeifer ,
J. W. da Silva Neto ,
L. T. Hax ,
M. M. Antunes ,
F. A. B. Del Pino ,
G. R. Paludo  and
M. N. Corrêa
A. Schneider*
Affiliation:
Biotechnology Center, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil Núcleo de Pesquisa, Ensino e Extensão em Pecuária (NUPEEC), Veterinary College, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil
L. F. M. Pfeifer
Affiliation:
Department of Veterinary Clinics, Veterinary College, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil Núcleo de Pesquisa, Ensino e Extensão em Pecuária (NUPEEC), Veterinary College, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil
J. W. da Silva Neto
Affiliation:
Department of Veterinary Clinics, Veterinary College, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil Núcleo de Pesquisa, Ensino e Extensão em Pecuária (NUPEEC), Veterinary College, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil
L. T. Hax
Affiliation:
Department of Veterinary Clinics, Veterinary College, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil Núcleo de Pesquisa, Ensino e Extensão em Pecuária (NUPEEC), Veterinary College, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil
M. M. Antunes
Affiliation:
Department of Veterinary Clinics, Veterinary College, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil Núcleo de Pesquisa, Ensino e Extensão em Pecuária (NUPEEC), Veterinary College, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil
F. A. B. Del Pino
Affiliation:
Department of Biochemistry, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil Núcleo de Pesquisa, Ensino e Extensão em Pecuária (NUPEEC), Veterinary College, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil
G. R. Paludo
Affiliation:
Department of Pathology, Veterinary College, University of Brasília, Campus Universitário Darcy Ribeiro, Asa Norte, CEP 70910-970, Brasília, DF, Brazil
M. N. Corrêa
Affiliation:
Department of Veterinary Clinics, Veterinary College, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil Núcleo de Pesquisa, Ensino e Extensão em Pecuária (NUPEEC), Veterinary College, Federal University of Pelotas, Campus Universitário, CEP 96010-900, Pelotas, RS, Brazil
*
†E-mail: augusto.schneider@live.com
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Abstract

The aim of this study was to investigate the effect of fasting and exogenous insulin administration on the expression of growth hormone receptor (GHR) and IGF-I mRNA in the pre-ovulatory follicle of ewes. Fifteen ewes received an intravaginal progesterone releasing device that was removed 6 days later (day of removal = day 0). On day −2, the ewes were divided into three groups: (i) fasting group (n = 5) that was fasted from day −2 to day 2; (ii) control group (n = 5) that received a maintenance diet; and (iii) insulin group (n = 5) that received insulin injections (0.25 IU/kg) every 12 h from day −2 to day 2 under the same diet as the control group. Follicular samples were obtained on day 2. Fasting increased plasma non-esterified fatty acids concentrations from day −1 to day 2 (P < 0.001). There was no difference (P > 0.05) in the number of follicles, although there was a tendency for an increase in the pre-ovulatory follicle diameter for the insulin group in comparison to the control group (P = 0.12). Thecal GHR mRNA expression was very low and was considered insignificant. Moreover, granulosa cells GHR mRNA expression increased (P < 0.05) in the insulin group. Expression of IGF-I mRNA was not different among groups in both tissues. In conclusion, insulin administration increases GHR mRNA but not IGF-I mRNA expression in granulosa cells of the pre-ovulatory follicle. However, fasting did not change the pattern of GHR/IGF-I mRNA expression in the pre-ovulatory follicle.

Keywords

GHRIGF-ImRNAovarysheep
Type
Full Paper
Information
animal , Volume 5 , Issue 9 , 05 August 2011 , pp. 1420 - 1425
Copyright
Copyright © The Animal Consortium 2011

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References

Adashi, EY 1998. The IGF family and folliculogenesis. Journal of Reproductive Immunology 39, 13–19.Google Scholar
Al-Mamun, M, Goto, K, Chiba, S, Sano, H 2009. Responses of plasma acetate metabolism to hop (Humulus lupulus L.) in sheep. International Journal of Biological Sciences 5, 287–292.Google Scholar
Alexander, BM, Kiyma, Z, McFarland, M, Van Kirk, EA, Hallford, DM, Hawkins, DE, Kane, KK, Moss, GE 2007. Influence of short-term fasting during the luteal phase of the estrous cycle on ovarian follicular development during the ensuing proestrus of ewes. Animal Reproduction Science 97, 356–363.Google Scholar
Bargouli, GG, Tsantarliotou, MP, Brozos, CN, Kokolis, NA, Boscos, CM 2007. Effect of norgestomet treatment on plasminogen activator activity in the cervical mucus and the endometrium in dairy cows. Journal of Veterinary Medicine Series A – Physiology, Pathology and Clinical Medicine 54, 393–397.Google Scholar
Bornfeldt, KE, Arnqvist, HJ, Enberg, B, Mathews, LS, Norstedt, G 1989. Regulation of insulin-like growth factor-I and growth hormone receptor gene expression by diabetes and nutritional state in rat tissues. Journal of Endocrinology 122, 651–656.CrossRefGoogle ScholarPubMed
Brameld, JM, Gilmour, RS, Buttery, PJ 1999. Glucose and amino acids interact with hormones to control expression of insulin-like growth factor-I and growth hormone receptor mRNA in cultured pig hepatocytes. Journal of Nutrition 129, 1298–1306.Google Scholar
Butler, ST, Marr, AL, Pelton, SH, Radcliff, RP, Lucy, MC, Butler, WR 2003. Insulin restores GH responsiveness during lactation-induced negative energy balance in dairy cattle: effects on expression of IGF-I and GH receptor 1A. Journal of Endocrinology 176, 205–217.Google Scholar
Cao, M, Buratini, J Jr, Lussier, JG, Carriere, PD, Price, CA 2006. Expression of protease nexin-1 and plasminogen activators during follicular growth and the periovulatory period in cattle. Reproduction 131, 125–137.Google Scholar
Cenci, FB, Louvandini, H, McManus, CM, Dell'Porto, A, Costa, DM, Araujo, SC, Minho, AP, Abdalla, AL 2007. Effects of condensed tannin from Acacia mearnsii on sheep infected naturally with gastrointestinal helminthes. Veterinary Parasitology 144, 132–137.Google Scholar
Cikos, S, Koppel, J 2009. Transformation of real-time PCR fluorescence data to target gene quantity. Analitical Biochemistry 384, 1–10.Google Scholar
Downing, JA, Scaramuzzi, RJ 1997. The effect of the infusion of insulin during the luteal phase of the estrous cycle on the ovulation rate and on plasma concentrations of LH, FSH and glucose in ewes. Theriogenology 47, 747–759.CrossRefGoogle ScholarPubMed
Eckery, DC, Moeller, CL, Nett, TM, Sawyer, HR 1997. Localization and quantification of binding sites for follicle-stimulating hormone, luteinizing hormone, growth hormone, and insulin-like growth factor I in sheep ovarian follicles. Biology of Reproduction 57, 507–513.CrossRefGoogle ScholarPubMed
Hastie, PM, Haresign, W 2010. Modulating peripheral gonadotrophin levels affects follicular expression of mRNAs encoding insulin-like growth factor binding proteins in sheep. Animal Reproduction Science 119, 198–204.Google Scholar
Hastie, PM, Onagbesan, OM, Haresign, W 2004. Co-expression of messenger ribonucleic acids encoding IGF-I, IGF-II, type I and II IGF receptors and IGF-binding proteins (IGFBP-1 to -6) during follicular development in the ovary of seasonally anoestrous ewes. Animal Reproduction Science 84, 93–105.CrossRefGoogle ScholarPubMed
Jones, JI, Clemmons, DR 1995. Insulin-like growth factors and their binding proteins: biological actions. Endocrine Reviews 16, 3–34.Google ScholarPubMed
Jorritsma, R, de Groot, MW, Vos, PL, Kruip, TA, Wensing, T, Noordhuizen, JP 2003. Acute fasting in heifers as a model for assessing the relationship between plasma and follicular fluid NEFA concentrations. Theriogenology 60, 151–161.CrossRefGoogle Scholar
Juengel, JL, Nett, TM, Anthony, RV, Niswender, GD 1997. Effects of luteotrophic and luteolytic hormones on expression of mRNA encoding insulin-like growth factor I and growth hormone receptor in the ovine corpus luteum. Journal of Reproduction and Fertility 110, 291–298.CrossRefGoogle ScholarPubMed
Khalid, M, Haresign, W, Luck, MR 2000. Secretion of IGF-1 by ovine granulosa cells: effects of growth hormone and follicle stimulating hormone. Animal Reproduction Science 58, 261–272.Google Scholar
Kosior-Korzecka, U, Bobowiec, R, Lipecka, C 2006. Fasting-induced changes in ovulation rate, plasma leptin, gonadotropins, GH, IGF-I and insulin concentrations during oestrus in ewes. Journal of Veterinary Medicine Series A – Physiology, Pathology and Clinical Medicine 53, 5–11.Google Scholar
Leeuwenberg, BR, Hurst, PR, McNatty, KP 1995. Expression of IGF-I mRNA in the ovine ovary. Journal of Molecular Endocrinology 15, 251–258.Google Scholar
Lucy, MC 2000. Regulation of ovarian follicular growth by somatotropin and insulin-like growth factors in cattle. Journal of Dairy Science 83, 1635–1647.Google Scholar
Lucy, MC, Bilby, CR, Kirby, CJ, Yuan, W, Boyd, CK 1999. Role of growth hormone in development and maintenance of follicles and corpora lutea. Journal of Reproduction and Fertility Supplement 54, 49–59.Google Scholar
Mackey, DR, Wylie, AR, Sreenan, JM, Roche, JF, Diskin, MG 2000. The effect of acute nutritional change on follicle wave turnover, gonadotropin, and steroid concentration in beef heifers. Journal of Animal Science 78, 429–442.CrossRefGoogle ScholarPubMed
Morimoto, S, Cerbon, MA, Alvarez-Alvarez, A, Romero-Navarro, G, Diaz-Sanchez, V 2001. Insulin gene expression pattern in rat pancreas during the estrous cycle. Life Sciences 68, 2979–2985.Google Scholar
NRC 1985. Nutrient requirements of sheep. National Academic Press, Washington, DC.Google Scholar
Perks, CM, ning-Kendall, PA, Gilmour, RS, Wathes, DC 1995. Localization of messenger ribonucleic acids for insulin-like growth factor I (IGF-I), IGF-II, and the type 1 IGF receptor in the ovine ovary throughout the estrous cycle. Endocrinology 136, 5266–5273.Google Scholar
Pfaffl, MW, Georgieva, TM, Georgiev, IP, Ontsouka, E, Hageleit, M, Blum, JW 2002. Real-time RT-PCR quantification of insulin-like growth factor (IGF)-1, IGF-1 receptor, IGF-2, IGF-2 receptor, insulin receptor, growth hormone receptor, IGF-binding proteins 1, 2 and 3 in the bovine species. Domestic Animal Endocrinology 22, 91–102.CrossRefGoogle ScholarPubMed
Puchala, R, Prieto, I, Banskalieva, V, Goetsch, AL, Lachica, M, Sahlu, T 2001. Effects of bovine somatotropin and thyroid hormone status on hormone levels, body weight gain, and mohair fiber growth of Angora goats. Journal of Animal Science 79, 2913–2919.Google Scholar
Radcliff, RP, McCormack, BL, Keisler, DH, Crooker, BA, Lucy, MC 2006. Partial feed restriction decreases growth hormone receptor 1A mRNA expression in postpartum dairy cows. Journal of Dairy Science 89, 611–619.CrossRefGoogle ScholarPubMed
Ramoun, AA, Osman, KT, Darwish, SA, Karen, AM, Gamal, MH 2007. Effect of pretreatment with insulin on the response of buffaloes with inactive ovaries to gonadotrophin-releasing hormone agonist treatment in summer. Reproduction, Fertility and Development 19, 351–355.Google Scholar
Rhoads, ML, Meyer, JP, Kolath, SJ, Lamberson, WR, Lucy, MC 2008. Growth hormone receptor, insulin-like growth factor (IGF)-1, and IGF-binding protein-2 expression in the reproductive tissues of early postpartum dairy cows. Journal of Dairy Science 91, 1802–1813.Google Scholar
Richards, MW, Wettemann, RP, Spicer, LJ, Morgan, GL 1991. Nutritional anestrus in beef cows: effects of body condition and ovariectomy on serum luteinizing hormone and insulin-like growth factor-I. Biology of Reproduction 44, 961–966.CrossRefGoogle ScholarPubMed
Russel, A 1991. Body condition scoring of sheep. In Sheep and goat practice (ed. E Boden), pp. 3–10. Bailliére Tindall, Oxford, UK.Google Scholar
Schoppee, PD, Armstrong, JD, Harvey, RW, Whitacre, MD, Felix, A, Campbell, RM 1996. Immunization against growth hormone releasing factor or chronic feed restriction initiated at 3.5 months of age reduces ovarian response to pulsatile administration of gonadotropin-releasing hormone at 6 months of age and delays onset of puberty in heifers. Biology of Reproduction 55, 87–98.Google Scholar
Simpson, RB, Chase, CC Jr, Spicer, LJ, Vernon, RK, Hammond, AC, Rae, DO 1994. Effect of exogenous insulin on plasma and follicular insulin-like growth factor I, insulin-like growth factor binding protein activity, follicular oestradiol and progesterone, and follicular growth in superovulated Angus and Brahman cows. Journal of Reproduction and Fertility 102, 483–492.Google Scholar
Smith, JF 1988. Influence of nutrition on ovulation rate in the ewe. Australian Journal of Biological Sciences 41, 27–36.Google Scholar
Spicer, LJ, Crowe, MA, Prendiville, DJ, Goulding, D, Enright, WJ 1992. Systemic but not intraovarian concentrations of insulin-like growth factor-I are affected by short-term fasting. Biology of Reproduction 46, 920–925.Google Scholar
Spicer, LJ, Echternkamp, SE, Wong, EA, Hamilton, DT, Vernon, RK 1995. Serum hormones, follicular fluid steroids, insulin-like growth factors and their binding proteins, and ovarian IGF mRNA in sheep with different ovulation rates. Journal of Animal Science 73, 1152–1163.Google Scholar
Underwood, LE, Murphy, MG 1987. Radioimmunoassay of the somatomedins. In Radioimmunoassay in basic and clinical pharmacology (ed. C Patrono), pp. 561–574. Springer-Verlog, Heinderberg, Germany.CrossRefGoogle Scholar
Vicini, JL, Buonomo, FC, Veenhuizen, JJ, Miller, MA, Clemmons, DR, Collier, RJ 1991. Nutrient balance and stage of lactation affect responses of insulin, insulin-like growth factor-I and factor-II, and insulin-like growth factor-binding protein-2 to somatotropin administration in dairy-cows. Journal of Nutrition 121, 1656–1664.Google Scholar
Viñoles, C, Forsberg, M, Banchero, G, Rubianes, E 2001. Effect of long-term and short-term progestagen treatment on follicular development and pregnancy rate in cyclic ewes. Theriogenology 55, 993–1004.Google Scholar
Whitley, NC, McFadin-Buff, EL, Keisler, DH 2000. Effect of insulin on feed intake and reproductive performance of well-nourished nulliparous ewes. Theriogenology 54, 1049–1054.Google Scholar